Resection of a left posterolateral thalamic cavernoma with the Nico BrainPath sheath: Case report, technical note, and review of the literature Academic research paper on "Clinical medicine"

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Interdisciplinary Neurosurgery: Advanced Techniques and

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Case report

Resection of a left posterolateral thalamic cavernoma with the Nico BrainPath sheath: Case report, technical note, and review of the literature

Peter S. Amenta *,1I Aaron S. Dumont1, Ricky Medel1

Tulane Medical Center, 1415 Tulane Avenue, New Orleans, LA 70112, United States

ARTICLE INFO ABSTRACT

Background: Management of symptomatic cavernomas of the posterolateral thalamus is particularly challenging due to their intimate relationship with the posterior limb of the internal capsule. The risk of continued observation and surgical resection is debilitating motor dysfunction. Traditional microsurgical approaches must be tailored for each lesion and account for the unique and specific anatomic relationships of individual cavernomas. Advances in neuronavigation, MRI, DTI, and tractography have improved the safety of these procedures. Unfortunately, resection remains associated with a significant risk of postoperative morbidity. Case description: We present a case report of a 44 year-old male with a symptomatic posterolateral thalamic cavernoma for which multiple microsurgical approaches were considered. Ultimately, a complete resection was achieved through a minimally invasive approach with the Nico BrainPath tubular retractor (Indianapolis, IN). Following a brief period of immediate postoperative right-sided hemiplegia, the patient had returned to near neurologic baseline at short-term follow-up.

Conclusion: We believe this to be the first report of a successful resection of a lesion in this anatomic location with this technology. Tubular retractor-guided approaches may represent a valid alternative when addressing cavernomas in this challenging region. Long-term follow-up and larger cases series are necessary to determine if outcomes are comparable to those associated with traditional microsurgical approaches.

© 2016 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license

(http://creativecommons.org/licenses/by-nc-nd/4.0/).

CrossMark

Article history: Received 22 March 2016 Accepted 27 March 2016 Available online xxxx

Keywords:

Basal ganglia cavernoma BrainPath Internal capsule Thalamic cavernoma Tubular retractor

1. Background

The management of cavernomas of the thalamus and basal ganglia is particularly challenging. Their proximity to, and sometimes involvement with, the genu and posterior limb of the internal capsule results in a significant risk of debilitating motor dysfunction, even in the setting of a relatively small hemorrhage [1-7]. Surgical resection is associated with a high risk of neurologic morbidity due to the manipulation and retraction of critical surrounding structures. Location in the dominant hemisphere results in additional risk of resection due to the possibility of a postoperative speech deficit [8]. As a result, observation of these lesions is indicated when asymptomatic or when found incidentally.

Unfortunately, a small subset of these lesions will behave aggressively, resulting in repeated hemorrhage and progressive neurologic deficit. Surgical resection in these cases is warranted to remove the future risk of progressive dysfunction and the risk of life-threatening

Abbreviations: DTI, diffusion tensor imaging; MRI, Magnetic resonance imaging; MEPs, motor evoked potentials; SSEPs, somatosensory evoked potentials. * Corresponding author. E-mail addresses: peter.amenta@gmail.com (P.S. Amenta), adumont2@tulane.edu (AS. Dumont), rmedel@tulane.edu (R. Medel).

1 No funding was received for the preparation of this manuscript.

hemorrhage [8,9]. Goals of resection are complete removal of the offending lesion and preservation of neurologic function at long-term follow-up [9,10]. The surgical approach must be tailored on an individual basis and take into account the exact location of the cavernoma and its relationship to surrounding structures. An array of microsurgical approaches have been used successfully in the treatment of these lesions. Advances in image guidance, diffusion tensor imaging (DTI), and tractography have allowed for more tailored and safer approaches to these lesions.

A 44 year-old male with a dominant hemisphere cavernoma centered in the posterolateral thalamus and displacing the genu and posterior limb of the left internal capsule presented on two separate occasions with right-sided hemiparesis. The patient made a significant recovery in function and was referred for radiosurgery. Significant weakness and growth of the hematoma occurred at the time of the third hemorrhage and surgical intervention was offered.

We present the first report of a posterolateral thalamic cavernoma successfully resected with the minimally invasive Nico BrainPath tubular retractor. Following a brief period of right hemiplegia and expressive aphasia in the immediate postoperative period, the patient experienced a rapid and dramatic recovery of neurologic function. At short-term follow-up, he had returned to near baseline motor strength and his aphasia was largely resolved. We believe that the tubular retractor

http://dx.doi.org/10.1016/j.inat.2016.03.006

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may offer a minimally invasive alternative to traditional microsurgical approaches for the management these challenging lesions. Obviously, a larger series of patients and long-term follow-up are required to determine if results are comparable to those obtained with traditional micro-surgical approaches.

2. Case report

2.1. Clinical history

A 44-year-old right-handed male presented to the clinic 6 weeks following the acute onset of mild right hand and leg weakness. At the time of presentation, the weakness had nearly resolved, however, the patient was left with incoordination in his right hand. Noncontrasted head CT demonstrated a mixed-density hemorrhagic mass in the lateral thalamus and posterior limb of the left internal capsule without surrounding edema. Magnetic resonance imaging (MRI) showed a 1.72 x 1.96 cm well-circumscribed mass and associated blood products consistent with a hemorrhagic cavernoma (Fig. 1). A diagnostic angiogram was negative for underlying vascular malformation. Observation was recommended, as the patient had made a near complete recovery.

Approximately 3 weeks after first presentation, the patient presented to the emergency room with new onset increased weakness in the right upper (4 -/5) and lower (4+/5) extremity. MRI demonstrated an increase in the size of the lesion, which now measured 2.4 x 2.6 cm. DTI and tractography confirmed that the mass was centered in the left lateral posterior thalamus and caused significant lateral displacement of the genu and posterior limb of the left internal capsule (Fig. 2). The patient rapidly recovered to near baseline motor function over the course of 48 h and he was referred for radiosurgery.

12 days later, prior to initiating radiotherapy, the patient presented a third time with 1/5 strength in the right hand, 3/5 strength in the proximal right upper extremity, and 4/5 strength in the right lower extremity. He also had developed mild right facial weakness. MRI again demonstrated a significantly larger lesion, now with a clearly defined 1.8 x 2.2 cm cavernoma and a surrounding 3.5 x 3 cm hematoma (Fig. 3). The patient was counseled on the risk of permanent paralysis with continued observation and radiosurgery. He was also informed of the significant risks of surgical resection, including, transient or permanent right hemiparesis or plegia and aphasia. The patient and family agreed to proceed with surgical resection.

22. Operative procedure

The patient was placed under general anesthesia and positioned supine on the operating table. Mannitol was not administered and

normocapnia was maintained until the obturator was passed through the white matter, as which point mild hyperventilation was performed. Neuromonitoring, including somatosensory evoked potentials (SSEPs) and motor evoked potentials (MEPs), was performed throughout the procedure. No identifiable left-sided MEPs were present with transcra-nial stimulation through scalp electrodes.

The head was fixed in the Mayfield three-point clamp and positioned parallel to the floor. Using Stealth neuronavigation the predetermined left frontal starting point was identified on the scalp. A linear paramedian incision was planned over the starting point. A small left frontal craniotomy was performed and an epidural lead was placed over the left motor strip. Left-sided MEPs were identified in the right deltoid and foot with stimulation through the epidural electrode. A small dural incision was made over the starting point and the target sulcus was identified. The sulcus was opened superficially with an arachnoid knife.

A 75 mm sheath was selected to traverse the 70 mm between the frontal starting point and the posterior inferior margin of the cavernoma. The obturator extends 15 mm beyond the distal end of the sheath and this distance must be incorporated into the planning. Using the Stealth navigation wand and obturator, the tubular retractor was advanced into position and secured to the Greenberg retractor. MEPs were immediately checked following trocar placement and the right deltoid and foot signals could no longer be identified through epi-dural stimulation.

The operating microscope was brought into the field and the hematoma was easily identified within the tubular retractor (Fig. 4). The hematoma and pieces of the cavernoma were removed systematically until the visualized field was clear. The tube was then progressively withdraw to allow additional hematoma and cavernoma to "fall" into the field. This process was repeated until the cavernoma and hematoma had been completely resected. The right deltoid and foot MEPs did not recover during the procedure, while SSEPs remained unchanged. Permanent section confirmed a cavernoma and associated hematoma.

The patient awakened in the operating room with a complete right hemiplegia, expressive aphasia, and a worsening right facial paralysis. Within 12 hours the patient improved to a 3/5 strength in the right upper extremity and 4 -/5 strength in the right lower extremity. His facial weakness recovered to baseline over the following 48 h. At the time of discharge 1 week later, he was ambulating with physical therapy. The proximal right upper and lower extremities had improved to 4+/5 strength. Unfortunately, the right hand remained plegic. MRI performed on postoperative day six demonstrated complete resection of the cavernoma, although this will require confirmation with repeat MRI in 3 to 6 months. Postoperative DTI and tractography demonstrated reduced mass effect on the posterior limb of the internal capsule (Fig. 5).

Fig. 1. MRI at presentation following first symptomatic hemorrhage. T1 (A) coronal and T2 (B) axial MRI demonstrating a 1.72 x 1.96 cm well-circumscribed lesion and associated blood products consistent with a hemorrhagic cavernoma. The cavernoma is centered in the lateral left thalamus and posterior limb of the internal capsule.

Fig. 2. MRI, DTI, and tractography following second symptomatic hemorrhage. (A) Gradient echo MRI demonstrating a 2.4 x 2.6 cm well-circumscribed hemorrhagic lesion without surrounding edema. (B) DTI shows the hemorrhage to be centered in the posterolateral thalamus. (C) Tractography confirms the intimate association with the tracts of the genu and posterior limb of the internal capsule, which are clearly displaced and bowed over the lateral margin of the hematoma.

3. Discussion

To the best of our knowledge, we report the first use of the BrainPath tubular retractor system for the resection of a cavernoma centered in the lateral thalamus and posterior limb of the internal capsule of the dominant hemisphere. Despite a loss of weak baseline MEPs in the operating room and an immediate postoperative hemiplegia, the patient demonstrated a rapid recovery of motor function in the upper and lower extremities. A moderate postoperative expressive aphasia had largely resolved at the time of discharge. Cavernomas of the thalamus and internal capsule present a challenging subset of lesions, for which management remains somewhat controversial. The risk of motor paralysis, and the potential speech deficit associated with dominant hemisphere lesions, once made these lesions largely inoperable. Microsurgical technique and advances in neuronavigation have made the deep supratentorial anatomy more accessible. The use of modern tubular retractors further increases the ease and speed of access, minimizes brain retraction, and displaces, rather than disrupts, deep and critical white matter tracts.

Fig. 3. MRI following third symptomatic hemorrhage. Following the third presentation, gradient echo MRI clearly demonstrated a distinct 1.8 x 2.2 cm cavernoma and a 3.5 x 3 cm surrounding hematoma.

3.1. Natural history and potential for recovery

The annual hemorrhage risk for asymptomatic cavernomas ranges between 0.39 and 4.2%, however, once symptomatic, the rebleed rate rises to 22.9% per patientyear [10-14]. These statistics are likely not entirely reflective of the actual hemorrhage rate, but in part, indicative of the proximity of symptomatic lesions to critical structures. Porter et al. also highlighted the effect of location on the rate of hemorrhage [2]. In 170 patient-years of observation, 4.1% of deep lesions were observed to bleed versus 0% of superficial lesions. Further impacting the poor natural history of cavernomas located in eloquent anatomy, is the low likelihood of full spontaneous recovery following a hemorrhage. Wostrack et al. reported a complete recovery following an initial hemorrhage in only 6 of 45 (13%) patients [15]. In patients with neurologic deficits treated nonsurgically, Porter and colleagues reported approximately two-thirds of patients achieved only partial or no recovery of function [2]. Multiple authors have published similar results pertaining to long-term outcome [16-19].

3.2. Surgical results

As was the case with our patient, resection of cavernomas in eloquent regions is associated with a significant risk of new or worsening neurologic deficits, particularly in the immediate postoperative period. This initial deterioration is due to manipulation and retraction of critical structures and the resultant edema [9]. In our case, the edema within the thalamus, internal capsule, and basal ganglia was clearly observed on the immediate postoperative scan. Adequate patient counseling prior to surgery is a key component of management in this case and the patient should be prepared to awaken with at least a transient worsening in condition. Our patient and his family were informed on the risk of right hemiplegia and the potential for a partial aphasia.

At follow-up, it is important to recognize that many patients do achieve a significant recovery of function. Bertalanffy et al. reviewed 26 patients treated with microsurgical resection of deep-seated cavernomas, 10 of which were located in the insula and basal ganglia [20]. Seven patients experienced a delayed recovery of function, while an additional eight suffered a significant complication. Wostrack et al. reported 47% of patients suffered a transient neurologic morbidity, with brainstem cavernomas associated with the highest rate of new neurologic deficit [15]. Importantly, 90% of patients harboring eloquent non-brainstem cavernomas had no new postoperative deficit and 50% of those patients exhibited improvement. In a series of 56 patients with symptomatic brainstem, thalamic, and basal ganglia AVMs, Steinberg et al. reported a worsened immediate postoperative neurologic deficit in 29% of patients. At the time of long-term follow-up, only 5% had a significant permanent deficit and 52% had improved compared to their presenting condition [9]. It is important to note that the

Fig. 4. Cavernoma resection with the Nico BrainPath tubular retractor. (A) Visualization of hematoma upon Stealth-guided placement of the Nico BrainPath sheath. (B) Resection of cavernoma with bimanual microsurgical technique. (C) The surrounding white matter is observed following complete cavernoma resection.

authors excluded cavernomas located solely in the posterior limb of the internal capsule due to the risk of permanent contralateral hemiplegia [9]. Large lesions of the basal ganglia and thalamus that extended into or displaced the posterior limb of the internal capsule were removed with good outcomes [9].

3.3. Traditional microsurgical options

The vast majority of literature pertaining to deep-seated supratentorial cavernomas is related to basal ganglia and thalamic lesions [3,8]. There is considerably less data in regards to cavernomas intimately associated with or within the posterior limb of the internal capsule. Multiple surgical approaches to this region have been described in the literature. The transsylvian transinsular approach is well-suited for insular and lateral basal ganglia lesions [21,22]. Cavernomas centered in the superomedial thalamus may be managed via the anterior interhemispheric contralateral transcallosal approach [23-25]. This approach is particularly appealing due to its avoidance of perforators and dissection of the Sylvian fissure. A transparietal transventricular approach allows for greater exposure of the lateral thalamus, but places the optic radiations at risk [26-28].

Posterior lesions centered near the midline are accessed via the posterior interhemispheric approach and its many variations [29]. The subcallosal approach adds additional lateral exposure to posterior lesions [9]. The supracerebellar infratentorial approach provides access to lesions arising in the posterior inferior thalamus [30]. Multiple authors have also described successful resection of posterior thalamic cavernomas through a parietooccipital transventricular approach that utilizes access through the pulvinar [3,8,9]. Transgression of the pulvinar has not resulted in significant morbidity in multiple reports [3,8,9].

These traditional approaches were discussed for the cavernoma described above, however, its location did not make any one approach particularly suitable. Spetzler specifically warns about the significant risk of surgical resection of cavernomas in the lateral aspect of the posterior thalamus [8]. The posterior limb of the internal capsule largely blocks lateral access, while access to the lesion is restricted in midline approaches. He suggests transsylvian transinsular or parieto-occipital approaches in these cases, but advises careful consideration when operating in the dominant hemisphere. In our case, the transsylvian transinsular approach was ruled out because it certainly would have required transgression of the fibers of the genu or posterior limb of the internal capsule. The profound effect that each hemorrhage had on motor function, highlighted the intimate relationship between the lesion and these motor fibers. Additionally, DTI and tractography showed the cavernoma and hematoma to be largely centered in the white matter tracts of the internal capsule.

The anterior interhemispheric contralateral transcallosal approach was not employed due to the significant mass of thalamus between the medial border of the lesion and the ventricle. The parietooccipital transventricular approach was felt to place the visual fibers, which are completely unaffected by the mass, at risk. The risk of a speech deficit with this approach and the transsylvian approach, due to working in the dominant hemisphere, was deemed high. The lesion did not approach the inferior thalamus, thus making the supracerebellar infratentorial approach a poor option.

3.4. ¡mage guidance

Advances in neuroimaging, including, high resolution MRI, DTI, and tractography have allowed for a greater understanding of the operative

Fig. 5. Postoperative imaging. (A) Immediate postoperative head CT demonstrating complete resection of left thalamic and internal capsule cavernoma. There is significant edema identified in the left thalamus, basal ganglia, and internal capsule. (B) Gradient echo MRI performed on postoperative day six demonstrates complete resection of the cavernoma and hematoma.

anatomy and for precise localization and planning of the surgical corridor for resection. Monitoring of MEPs and SSEPs allow for realtime feedback.

3.5. Tubular retractors

Tubular retractors, along with frame-based navigation, were first used by Kelly and colleagues for the resection of deep-seated tumors [31-33] Advances in frameless stereotaxy have since led to the advent of multiple frameless tubular retractor systems [31-36]. The Nico BrainPath tubular sheath system has been shown to be safe and effective in its ability to access intracerebral hematomas located in deep-seated or eloquent regions [37]. The obturator features a tapered end which promotes displacement of the white matter tracts, rather than transection, during advancement of the system to the target. This approach, first described by Ritsma and colleagues, has been termed minimally invasive subcortical parafascicular transulcal access [37].

The sheath is manufactured in three lengths (50 mm, 60 mm, 75 mm) to allow for tailored access depending on the depth of individual lesions. All sheaths are a standardized 13.5 mm in diameter, which allows for bimanual dissection and clear visualization through the operating microscope. The sheath is composed of clear plastic that allows for visualization of the surrounding anatomy. Placement of the sheath at the most inferior pole of the lesion holds overlying tissue out of the field of view and allows for the systemic clearing of pathology. Once the visualized area has been cleared, the sheath is "backed-out" to allow overlying lesional tissue to "fall" into the field. This process is repeated until the pathology is resected and the sheath has been removed beyond the most superficial surface of the lesion. An estimation of the involvement of surrounding tissue can be gleaned from direct visualization through the clear sheath.

Compared to traditional microsurgical techniques, there are a number of important differences in technique that are critical to the success of tubular retractor approaches. Whereas traditional microsurgical and skull base approaches rely heavily on brain relaxation, resection with a tubular retractor is aided by maintaining a "full" brain. Osmotic diuretics are avoided and normocapnia is maintained. These measures prevent the brain from sagging, which increases the accuracy of neuronavigation. We employ a brief period of hyperventilation just prior to sheath and obturator insertion to account for the added volume of the tube. The normal to slightly elevated intracranial pressure also drives the lesion, particularly hematomas, into the sheath. This phenomenon delivers the mass to the surgeon and limits dissection off of critical structures. A small dural opening, only large enough to safely pass the sheath without resistance, is also critical. The minimal opening creates a seal around the tube that maintains the intracranial pressure and stabilizes the sheath during resection.

We feel that the tubular sheath offered distinct advantages over traditional microsurgical approaches in this case. First, the sheath obviated the need for dissection of the Sylvian and interhemispheric fissures. Second, the selected trajectory passed medial to the arcuate fasciculus and entered the hematoma cavity above the level of the majority of the internal capsular fibers. Third, the hematoma largely delivered itself into the tube and was easily removed with irrigation and gentle suction, minimizing white matter dissection. Fourth, the maintenance of normal to slightly increased intracranial pressure aided significantly in hemo-stasis. As the tube was progressively retracted, the white matter collapsed on itself, thereby tamponading the cavity. Minimal bipolar cautery was required, which is critical in eloquent areas. Finally, a small craniotomy through a linear incision was all that was required for adequate access. Operative time and blood loss was also limited to approximately 2 h and 50 cm3, respectively.

There are certainly some disadvantages to the minimally invasive approach employed in this case. Although the Nico BrainPath retractor does allow for some "toggling" to view different areas of the resection cavity, we specifically avoided this maneuver. Do the belief that we

were passing through at least some component of the genu and posterior limb of the internal capsule, we did not want to apply undue tor-sional stress to the critically important motor fibers. Instead, we relied entirely on the tendency of the lesion to "fall" into the field and maintained a perpendicular orientation throughout the case. As a result, we were somewhat limited in our field of view, which could have led to incomplete resection. Residual cavernomas in eloquent areas are known to follow an aggressive course, resulting in repeated hemorrhage, enlargement, and worsening neurologic deficits [9,20]. Fortunately, postoperative MRI is consistent with complete removal, but repeat imaging at 3 to 6 months is required to confirm curative resection.

The second main disadvantage of the sheath retractor was the long tract that was required to reach the lesion. Without a doubt, the retractor passed through components of the basal ganglia and the displaced fibers of the internal capsule, which was reflected in the immediate loss of weak MEPs. Although the sheath and obturator are specifically designed to displace the fibers, there is no way to quantify the damage, or lack of damage, imposed during sheath placement. Additional studies both in the lab and in clinical practice are required to better define this variable.

3.6. Limitations

Clearly, additional patients with similarly located lesions will need to be treated to determine the benefit of the tubular retractor approach to cavernomas of the posterior limb of the internal capsule. The rarity of these lesions will make the accumulation of significant data challenging. Of course, we do not know if the outcome would have been improved with traditional microsurgical resection. It is also important to point out that this lesion was exhibiting a hemorrhage pattern consistent with temporal clustering [38]. There is a possibility that the lesion may have become less inclined to bleed with time, responded to radio-surgery, and the patient would have made a significant recovery. The patient was counseled in regards to this option, but do to the aggressive clinical course and progressive motor deficit with each hemorrhage, complete surgical resection was indicated.

4. Conclusion

Resection of cavernomas of the posterolateral thalamus, due to their intimate relationship with the posterior limb of the internal capsule, represent the greatest surgical challenge of the supratentorial deep-seated cavernomas. The risk of significant morbidity is further increased when located in the dominant hemisphere. In this case, successful complete resection of the lesion was achieved with the minimally invasive Nico BrainPath retractor. Although this retractor, and others like it, have been used successfully with other lesion, this is the first report of a cavernoma resection in this very specific anatomic location. The patient experienced immediate postoperative deterioration, but improved rapidly and has returned to near neurologic baseline at short-term follow-up. We believe that the Nico system represents a potential viable surgical option when addressing these lesions. Long-term follow-up and larger patient series will be necessary to determine if outcomes are comparable to those achieved with traditional microsurgical approaches.

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